MADS-box genes
From Purdue Genomics Database Facility
Elizabeth Barker (barker1e@uregina.ca), Lydia Gramzow (lydia.gramzow@uni-jena.de), Barbara Ambrose (b.ambrose@massey.ac.nz), Christian Schulz (Christian.Schulz-3@ruhr-uni-bochum.de), Neil Ashton (physcomitrella@gmail.com), Guenter Theissen (Guenter.Theissen@uni-jena.de) and Amy Litt (alitt@nybg.org)
Contents |
Summary
• Many important aspects of plant morphogenesis, including evolution and specification of the architecture of both vegetative and generative parts, are controlled by members of multigene families that encode transcription factors. Arguably the most significant of these is the MADS-box gene family. Selaginella moellendorffii is currently the only lycophyte or, indeed, vascular cryptogam whose genome has been fully sequenced. Examination of the genome revealed 19 putative MADS-box genes, a number that is comparable to that in Physcomitrella and intermediate between those of the green algae and the angiosperms.
• Phylogenetic reconstructions demonstrated that there are few supported clades comprising genes from both seed plants (spermatophytes) and non-seed plants. However evidence suggests that M alpha genes are present in all land plants and a member of this group has been implicated in female gametophytic or embryonic development in Arabidopsis.
• None of the Selaginella MIKCC genes are orthologs of any of the floral homeotic genes. The expansion of this subfamily in the lineage leading to seed plants was almost certainly required for evolution of their unique reproductive organs.
• Selaginella and angiosperms possess noticeably fewer MIKC* genes than Physcomitrella. Some angiosperm MIKC* genes have been shown to be expressed in gametophytes and to play a role in gametophytic development. Consequently, it is plausible that Selaginella is less well represented that Physcomitrella because it has a reduced (relative to Physcomitrella) gametophytic stage in its life cycle.
• The absence of MIKC genes in algal chlorophytes and the acquisition and considerable expansion of the MIKC subfamily in the lineage leading from green algae, via charophytes, to bryophytes and lycophytes (Fig. 1) may have been required for evolution of the terrestrial plant body and successful colonisation of land.
Background
Many important aspects of plant morphogenesis, including the evolution and specification of the architecture of both vegetative and generative parts, are controlled by members of multigene families that encode transcription factors. Arguably the most significant of these is the MADS-box gene family. Members of this family are found in almost all eukaryotes, but their numbers have increased dramatically only during plant evolution. Whereas animals and fungi have approximately 2-6 MADS-box genes, Physcomitrella has 26 [39] and Arabidopsis possesses over 100 [27, 34]. The discovery of MADS-box genes in non-flowering plants, including conifers, a gnetophyte, ferns, lycophytes and a moss [13, 21, 41 and references therein] has fueled a resurgence of interest in plant “evo-devo”, the close relationship between evolution and development. Now availability of the whole genome sequences for three green algae, Physcomitrella, Selaginella and three flowering plants offers access to their complete complements of MADS-box genes and, when combined with gene function studies, should enable a more profound comprehension of the evolution of MADS-box genes and their functions as well as of the evolution of the various major land plant groups and structures, such as angiosperm floral organs, which define each of them.
All MADS-domain proteins possess the strongly conserved 58-60 amino acid MADS DNA-binding domain at or near the N terminus of the protein. The proteins are classified into two groups, Type I (Mα, Mβ, Mγ) and Type II (MIKCC and MIKC*, also known as Mδ) based on structure and sequence analyses [1, 27, 34]. Little is known about the functions of Type I MADS-domain proteins in plants, even though they outnumber Type II in Arabidopsis (Fig. 1) [8, 27, 34]. Arabidopsis FEM111 (AGL80) [36] and PHERES1 (AGL37) [19, 20], both Mγ genes, as well as the Mα genes, AGL23 [7] and AGL62 [16], are the only functionally characterized Type I MADS-box genes out of approximately 60 present in the Arabidopsis genome. All are required for proper female gametophyte (embryo sac) and/or endosperm development. In contrast, nearly 50 % of Type II MADS-box genes present in the Arabidopsis genome have been studied in depth, as many are key regulators of flowering time, floral organ identity, and fruit development (e.g., [2, 4, 5, 9, 10, 14, 15, 22, 24-26, 28, 35]). In addition, many of these Type II MADS-box genes may be conserved in function across the angiosperms. Most of the major clades of angiosperm Type II genes are also found in gymnosperms, but have not yet been detected in ferns, lycophytes, or mosses [6, 12, 13, 21, 29, 30, 42, 43, 45]. Thus Type II MADS-box genes appear to have diversified independently in seed plants.
Type II (MIKC) MADS-domain proteins found in plants are characterized by a second diagnostic region, the structurally conserved K domain [1, 17, 27]. Characterized by evenly spaced hydrophobic residues, this domain is predicted to form a coiled-coil that resembles keratin, and is implicated in dimerization and higher order protein interactions [25]. The MADS and K domains are separated by a short intervening (I) domain that also plays a role in protein interactions [40]. It is conserved among closely related proteins but in general the sequence is not strongly conserved. The C terminal domain of Type II MADS-domain proteins is highly variable, even among recently diverged sequences. It mediates higher order protein complex formation, and in specific cases, confers activities such as protein modification or transcription activation.
Analysis of MIKC proteins from Physcomitrella uncovered a further subdivision into two subgroups [13]. MIKC* sequences possess a significantly longer I domain than MIKCC (“classic”) sequences (60-80 amino acids and approximately 35 respectively). Additionally, in MIKC* genes the K domain is more variable in sequence and structure and consequently may be difficult to recognize [13]. MIKC* genes are not well characterized, but several angiosperm MIKC* genes appear to play important roles in male gametophyte (pollen) development [18, 49, 50]. In contrast, angiosperm MIKCC genes include those that play key roles in flowering and in fruit development, and consequently a great many are extremely well studied.
Figure 1: Comparison of the numbers of Type I, MIKCC and MIKC* MADS-box genes in the seven fully sequenced plant genomes including Ostreococcus lucimarinus [33], O. tauri [48], Chlamydomonas reinhardtii [44], Physcomitrella patens [39], Selaginella moellendorffii, Arabidopsis thaliana [34], Oryza sativa (rice) [3] and Populus trichocarpa [23]. Slightly different numbers of MADS-box genes have been reported for Arabidopsis [27, 32] and rice [11, 32].
MADS-box genes in S. moellendorffii
Selaginella moellendorffii is currently the only lycophyte or, indeed, vascular cryptogam whose genome has been fully sequenced (Table 1). Examination of the genome reveals 19 putative MADS-box genes. A multiple alignment of the corresponding MADS-domains is shown in Fig. 2. Two additional potential loci (MADS16 and MADS21, not included in this analysis) are problematic and require further analysis. Based on sequence alignment and phylogenetic analysis, two-thirds (13) appear to be Type I. Most of these lack EST data, and some are located in highly repetitive regions (Table 1); thus the status of these as transcribed, functional genes remains to be verified. Of the six Selaginella Type II sequences, three are MIKCC , whereas the remaining three are MIKC* (Fig. 1, Table 1).
Figure 2: Alignment of the MADS-domains of 19 putative MADS-domain transcription factors identified in Selaginella moellendorffii (MADS1–15, MADS17-20) and three MADS-domains from MADS-domain transcripton factors of Arabidopsis thaliana (AGAMOUS (MIKCC), AGL65 (MIKC*), AGL23 (Type I).
Whereas the Selaginella and Arabidopsis genomes have considerably more Type I than Type II genes, the opposite is true of the Physcomitrella genome (Fig. 1). Within the Type II group, Physcomitrella has twice as many MIKC* genes as MIKCC , Selaginella has equal numbers, and Arabidopsis has over six times as many MIKCC genes as MIKC*. Populus and Oryza, the other two sequenced angiosperm species, have different proportions of Type I and Type II, however, all three angiosperm taxa possess approximately seven times as many MIKCC as MIKC* genes. (Fig. 1).
Table 1 below lists all 19 Selaginella MADS-box genes, designation as Type I, MIKCC , or MIKC*, number of exons, domains identified, and presence of EST data.
| Gene | Type | Protein ID and Scaffold address | Exons | Domains | EST evidence | Notes |
| MADS1 | MIKCC | MADS1-1 450804 35:358419-361058; MADS1-2 450837 41:1167560-1170242 | 8 | NMIKC | Yes | |
| MADS2 | MIKC* | MADS2-1 450867 3:2290112-2292855; MADS2-2 451128 25:969915-972228 | 10 | MIKC | Yes | |
| MADS3 | MIKCC | MADS3-1 449545 64:822257-824884; MADS3-2 449594 70:921340-923666 | 7 | MIKC | Yes | |
| MADS4 | MIKC* | MADS4-1 449720 47:692864-694493; MADS4-2 449721 54:579008-580632 | 11 | MIKC | No | |
| MADS5 | Type I | MADS5-1 450771 1:2724519-2725654; MADS5-2 411869 16:1384664-1385740 | 1 | MC | Yes | |
| MADS6 | MIKCC | MADS6-1 450818 87:578224-579570; MADS6-2 450937 119:43718-45062 | 7 | MIKC | No | |
| MADS7 | Type I (Mγ) | MADS7-1 450800 15:1974936-1975961; MADS7-2 450939 115:313400-314425 | 1 | MC | No | |
| MADS8 | Type I | MADS8-1 411193 14:1546925-1547530; MADS8-2 418359 37:1530218-1530823 | 1 | MC | No | |
| MADS9 | Type I | MADS9-1 450769 14:1482769-1483497; MADS9-2 451046 37:1500689-1501393 | 1 | MC | No | |
| MADS10 | MIKC* | MADS10-1 450980 14:588969-590252; MADS10-2 450991 37:486640-487932 | 9 | MIKC | No | |
| MADS11 | Type I | MADS11-1 450768 7:2755684-2756604; MADS11-2 451047 36:1003871-1004800 | 1 | MC | No | |
| MADS12 | Type I | MADS12-1 449663 12:1935933-1936554; MADS12-2 449669 15:794114-794734 | 2 | NMC | No | |
| MADS13 | Type I | MADS13-1 411173 14:1448322-1448795; MADS13-2 418341 37:1466798-1467304 | 1 | MC | No | |
| MADS14 | Type I (Mα) | MADS14-1 450777 9:242419-243051; MADS14-2 450776 50:1095903-1096535 | 1 | MC | No | |
| MADS15 | Type I (Mα) | MADS15-1 450773 24:1347352-1348006; MADS15-2 450775 69:912520-913137 | 1 | MC | No | MADS15-2 appears to be a misassembled amalgam of MADS15 and MADS16 |
| MADS17 | Type I | MADS17-1 450647 42:249276-250358; MADS17-2 450646 67:484711-485793 | 1 | MC | No | |
| MADS18 | Type I | MADS18-1 450651 23:96633-97385; MADS18-2 450652 58:977778-978527 | 2 | NMC | No | |
| MADS19 | Type I | MADS19-1 450654 20:1962924-1963588; MADS19-2 450662 62:720731-721395 | 2 | NMC | No | Sequence is within long terminal repeats |
| MADS20 | Type I | MADS20-1 450653 21:946094-946882; MADS20-2 450659 31:782257-783045 | 1 | NMC | No | Sequence is within long terminal repeats |
Table 2. List of MADS-box genes found in the genome of Selaginella moellendorffii. Designation as Type I, MIKCC , and MIKC*, or unclassified is based on structure and phylogenetic analysis.
Evolutionary and functional implications
Only one MADS-box gene has been found in each of three Charophycean green algae, the closest relatives of land plants, so it is clear that the MADS-box gene family expanded considerably throughout the 480 MY or so of land plant evolution [44]. However, the Selaginella genome has approximately 25% fewer MADS-box genes than the genome of Physcomitrella and, as noted earlier, the proportions of Type I and Type II genes are essentially reversed. The relative contributions of gene loss and gain to these changes are unknown. Our phylogeny reconstructions (Fig. 3) favor a scenario in which the most recent common ancestor of land plants had relatively few MADS-box genes, possibly only one as in the charophytes. Subsequently there appears to have been a greater relative expansion of Type I genes in the tracheophyte lineage (lycophytes + ferns + seed plants) than in the moss lineage, while the reverse was true for Type II genes. Previous studies [1] that included MADS-box genes from animals as well as plants suggested that Type I and Type II MADS-box genes each formed single clades, and that the divergence of these two clades predated the split between the animal and plant lineages. Our analyses (Fig. 3) do not support this hypothesis, showing support only for the Type I gene clade, which appears in our topologies to be derived from Type II. This would imply a separate origin of Type I genes in animals and plants, and would suggest that the designation “Type I” reflects sequence characteristics that were convergently evolved. This question must be addressed with a dataset that includes animal, fungus, and plant Type I and Type II genes.
Fig. 3. Phylogenetic tree of MADS-box genes constructed using the maximum likelihood (ML) method as implemented in the program RAxML. The analysis is based on an alignment of the MADS-box sequences of the corresponding genes. Bold branches indicate clades that were found in all of our trees constructed using ML, maximum parsimony (MP, as implemented in the program TNT) and Bayesian analysis (as implemented in MrBayes). Medium branches designate clades that were found in two out of these three trees, and light branches indicate clades found only in the ML tree. Bootstrap and jacknife percentages and posterior probabilities for the ML, MP and Bayesian trees are indicated at each node in this order. Type I (red), MIKCC (green) and MIKC* (blue) MADS-box genes are differentiated by colors.
Fig. 4. Phylogenetic tree of MIKC* genes constructed using the maximum likelihood (ML) method as implemented in the program RAxML. The analysis is based on an alignment of the MADS, I, and K domains of the corresponding genes. Bold branches indicate clades that were found in all of our trees constructed using ML, maximum parsimony (MP, as implemented in the program TNT) and Bayesian analysis (as implemented in MrBayes). Medium branches designate clades that were found in two out of these three trees, and light branches indicate clades found only in the ML tree. Bootstrap and jacknife percentages and posterior probabilities for the ML, MP and Bayesian trees are indicated at each node in this order.
Fig. 5. Phylogenetic tree of MIKCC genes constructed using the maximum likelihood (ML) method as implemented in the program RAxML. The analysis is based on an alignment of the MADS, I, and K domains of the corresponding genes. Bold branches indicate clades that were found in all of our trees constructed using ML, maximum parsimony (MP, as implemented in the program TNT) and Bayesian analysis (as implemented in MrBayes). Medium branches designate clades that were found in two out of these three trees, and light branches indicate clades found only in the ML tree. Bootstrap and jacknife percentages and posterior probabilities for the ML, MP and Bayesian trees are indicated at each node in this order.
Phylogeny reconstructions involving the MADS-box genes of S. moellendorffii together with informative sets of MADS-box genes from other completely sequenced plant genomes (Arabidopsis thaliana, Oryza sativa, Physcomitrella patens) reveal few supported clades comprising genes from both seed plants (spermatophytes) and non-seed plants (Fig. 3). Nonetheless, sequence analysis indicates that Mα Type I genes are found in all sequenced land plant genomes (Physcomitrella, Selaginella and angiosperms); the inability of our phylogenetic analyses to recover this clade is likely an artifact of taxon sampling and insufficient alignable sequence. Thus an Mα gene probably already existed in the most recent common ancestor of mosses and vascular plants about 450 MYA [47]. Together with recent data from Arabidopsis [7] this suggests an ancient and potentially highly conserved function of Mα genes, possibly in female gametophytic or embryonic development.
Although in our analysis the Type II MADS-box genes do not form a single clade, the MIKC* genes do consistently form a clade that includes Physcomitrella, Selaginella, and angiosperm genes (Figs. 3 & 4). Within this clade, the Physcomitrella genes form a distinct clade, suggesting possible independent diversification of this group in mosses. In Arabidopsis, MIKC* MADS-box genes have been shown to be expressed in gametophytes and to play a role in gametophytic development. Physcomitrella has a gametophyte-dominant life-cycle, which may be related to the apparent expansion of the MIKC* genes in this group. In contrast, the gametophyte of Selaginella is highly reduced relative to Physcomitrella, which may account for fewer MIKC* genes in the former. However there are no additional taxa with enough data to determine if this represents losses in Selaginella, duplications in Physcomitrella, or both.
Most importantly, orthologous relationships between floral homeotic genes from angiosperms and any of the MIKCC genes from S. moellendorfii could not be detected (Figs. 3 & 5). Previous analyses had already suggested that orthologs of some floral homeotic genes are present in gymnosperms, but are absent from non-seed plants such as mosses and ferns (e.g. [4, 5, 12, 13, 21, 29, 30, 42, 43, 46, 47]). This suggested that the clades of floral homeotic genes were established 300 – 400 MYA, i.e. before the radiation of extant seed plants, but after the lineage that led to extant ferns had branched off [6, 46]. In contrast, molecular clock analyses suggested that some clades of MIKCC -type genes found in angiosperms are considerably older, and that ‘floral’ MADS-box genes might have originated even more than 800 MYA, thus by far predating the best estimates for the origin of the land plants [31, 37]. Explanations for this discrepancy include massive gene loss during evolution, dramatic sequence divergence and incompleteness of the fossil record of land plants (which appear to us unlikely to explain the phenomenon), and incomplete gene sampling, which may have led to an underestimation of the ages of the gene clades known from angiosperms and gymnosperms [31]. The analysis of the genome of P. patens [39] debunked that argument already for mosses. Our analyses of the S. moellendorffii genome now suggest that the clades of floral homeotic genes and other MIKCC -type genes known from angiosperms originated not earlier than the separation of the lineage that led to ferns (sensu lato) and seed plants from the lycophytes 400 – 450 MYA. Whether there are such genes in ferns remains to be seen, but appears to us unlikely. We hypothesize that the molecular clock estimates overestimated the age of the floral homeotic gene clades because mutation rates in this complex gene family comprising many paralogous genes may have been higher during early stages of MADS-box gene evolution (or even after every round of whole genome duplication) than during more recent phases, a possibility already considered by Nam et al.[31].
Given the ubiquitous presence of MADS-box genes in embryophytes together with what we know already about their important roles in the development and evolution of spermatophytes, it is clear that we should now afford the highest priority to functional analyses of the complete MADS-box gene complement discerned within the Selaginella genome. It will be interesting to discover, for example, whether any of the Selaginella genes encode a reproductive function as has been shown for some MIKCC genes in Physcomitrella [38, 41] and two charophycean algae [44].
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